Anatomical Correlates of Sentence Comprehension and Verbal Working Memory in Neurodegenerative Disease

This study investigates whether sentence comprehension and nonsyntactic verbal working memory (vWM) are sustained by the same or by different neural systems. Scores in a sentence–picture matching task and in digits backward (DB) were correlated with magnetic resonance imaging voxelwise gray matter volumes using voxel-based morphometry in 58 patients with neurodegenerative diseases. Results showed that overall sentence comprehension scores, regardless of grammatical structure, correlated with gray matter volumes in the left temporoparietal region, whereas DB scores correlated with dorsolateral prefrontal and inferior parietal volumes. Comprehension of multiclausal relative sentences (type 3) significantly correlated with voxels in the dorsal portion of the left inferior and middle frontal gyri. When DB and multiclausal relative sentences were directly compared, they showed overlapping neural substrates in the dorsolateral left frontal region, supporting a single source of vWM for syntactic and nonsyntactic tasks. Within this large area of common involvement, a small portion of pars triangularis showed an independent effect of multiclausal sentences, whereas a region in the middle frontal gyrus showed greater correlation with DB. This study reconciles two opposing views, which hold that sentence comprehension and vWM rely on either the same or different anatomical resources.

[1]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

[2]  J. Gee,et al.  Neural basis for sentence comprehension: Grammatical and short‐term memory components , 2002, Human brain mapping.

[3]  M. Grossman,et al.  A longitudinal study of sentence comprehension difficulty in primary progressive aphasia , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[4]  Edward E. Smith,et al.  Working Memory: A View from Neuroimaging , 1997, Cognitive Psychology.

[5]  Howard J. Rosen,et al.  Distinctive Neuropsychological Patterns in Frontotemporal Dementia, Semantic Dementia, And Alzheimer Disease , 2003, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[6]  Karl J. Friston,et al.  Automatic Differentiation of Anatomical Patterns in the Human Brain: Validation with Studies of Degenerative Dementias , 2002, NeuroImage.

[7]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[8]  I Litvan,et al.  Which clinical features differentiate progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) from related disorders? A clinicopathological study. , 1997, Brain : a journal of neurology.

[9]  R. E. Passingham,et al.  Sequencing ability in Parkinsonians, patients with frontal lobe lesions and patients who have undergone unilateral temporal lobectomies , 1989, Neuropsychologia.

[10]  S. Bookheimer,et al.  Dissociating Neural Mechanisms of Temporal Sequencing and Processing Phonemes , 2003, Neuron.

[11]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

[12]  A. Dale,et al.  Distinct Patterns of Neural Modulation during the Processing of Conceptual and Syntactic Anomalies , 2003, Journal of Cognitive Neuroscience.

[13]  A. A. Wijers,et al.  Localizing components of a complex task: sentence processing and working memory , 1998, Neuroreport.

[14]  R. Cabeza,et al.  Handbook of functional neuroimaging of cognition , 2001 .

[15]  D. Swinney,et al.  An On-Line Analysis of Syntactic Processing in Broca′s and Wernicke′s Aphasia , 1993, Brain and Language.

[16]  Karl J. Friston,et al.  Why Voxel-Based Morphometry Should Be Used , 2001, NeuroImage.

[17]  A. Friederici,et al.  Auditory Language Comprehension: An Event-Related fMRI Study on the Processing of Syntactic and Lexical Information , 2000, Brain and Language.

[18]  A. Caramazza,et al.  Dissociation of algorithmic and heuristic processes in language comprehension: Evidence from aphasia , 1976, Brain and Language.

[19]  Howard J. Rosen,et al.  The Anatomy of Category-specific Object Naming in Neurodegenerative Diseases , 2006, Journal of Cognitive Neuroscience.

[20]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[21]  M. Just,et al.  Brain Activation Modulated by Sentence Comprehension , 1996, Science.

[22]  M. Onofrj,et al.  Diagnosis and management of dementia with Lewy bodies: Third report of the DLB Consortium , 2006, Neurology.

[23]  Andrea Moro,et al.  Neural Correlates for the Acquisition of Natural Language Syntax , 2002, NeuroImage.

[24]  M. Just,et al.  From the SelectedWorks of Marcel Adam Just 1992 A capacity theory of comprehension : Individual differences in working memory , 2017 .

[25]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[26]  N. Dronkers,et al.  Lesion analysis of the brain areas involved in language comprehension , 2004, Cognition.

[27]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[28]  C. Grady,et al.  Behavioural and neural changes after phonological treatment for anomia , 2006, Brain and Language.

[29]  David Caplan,et al.  Effects of Syntactic Structure and Propositional Number on Patterns of Regional Cerebral Blood Flow , 1998, Journal of Cognitive Neuroscience.

[30]  G. Waters,et al.  Activation of Broca's area by syntactic processing under conditions of concurrent articulation , 2000, Human brain mapping.

[31]  Isabell Wartenburger,et al.  Neural correlates of syntactic transformations , 2004, Human brain mapping.

[32]  Cathy J. Price,et al.  Functional Neuroimaging of Language , 2001 .

[33]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[34]  D. Caplan,et al.  Sentence Comprehension in Patients with Alzheimer′s Disease , 1994, Brain and Language.

[35]  N Makris,et al.  Location of lesions in stroke patients with deficits in syntactic processing in sentence comprehension. , 1996, Brain : a journal of neurology.

[36]  Karl J. Friston,et al.  Voxel-based morphometry , 2007 .

[37]  Yosef Grodzinsky,et al.  Neural correlates of syntactic movement: converging evidence from two fMRI experiments , 2004, NeuroImage.

[38]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[39]  M. Weiner,et al.  Cognition and anatomy in three variants of primary progressive aphasia , 2004, Annals of neurology.

[40]  William F. Eddy,et al.  Time Course of fMRI-Activation in Language and Spatial Networks during Sentence Comprehension , 1999, NeuroImage.

[41]  C. Price.  The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[42]  D. Shankweiler,et al.  An Event-related Neuroimaging Study Distinguishing Form and Content in Sentence Processing , 2000, Journal of Cognitive Neuroscience.

[43]  C. Fiebach,et al.  Revisiting the role of Broca's area in sentence processing: Syntactic integration versus syntactic working memory , 2005, Human brain mapping.

[44]  David Caplan,et al.  Localization of Syntactic Comprehension by Positron Emission Tomography , 1998, NeuroImage.

[45]  M. D’Esposito,et al.  Language comprehension profiles in Alzheimer's disease, multi-infarct dementia, and frontotemporal degeneration , 1996, Neurology.

[46]  D. Wechsler.  Wechsler Adult Intelligence Scale , 2021, Encyclopedia of Evolutionary Psychological Science.

[47]  Irene Litvan,et al.  Corticobasal degeneration and its relationship to progressive supranuclear palsy and frontotemporal dementia , 2003, Annals of neurology.

[48]  G. Waters,et al.  Working Memory and On-Line Sentence Comprehension in Patients with Alzheimer's Disease , 1997, Journal of psycholinguistic research.

[49]  A D Friederici,et al.  Syntactic Working Memory and the Establishment of Filler-Gap Dependencies: Insights from ERPs and fMRI , 2001, Journal of psycholinguistic research.

[50]  D. Caplan,et al.  Syntactic determinants of sentence comprehension in aphasia , 1985, Cognition.

[51]  Guido F. Schauer,et al.  Neuroanatomical correlates of behavioural disorders in dementia. , 2005, Brain : a journal of neurology.

[52]  G. Waters,et al.  Verbal working memory and sentence comprehension , 1999, Behavioral and Brain Sciences.

[53]  R. Faber,et al.  Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. , 1999, Neurology.

[54]  J. Gee,et al.  Large-scale neural network for sentence processing , 2006, Brain and Language.

[55]  Richard S. J. Frackowiak,et al.  The role of the right hemisphere in the interpretation of figurative aspects of language. A positron emission tomography activation study. , 1994, Brain : a journal of neurology.

[56]  E. Kaan,et al.  The brain circuitry of syntactic comprehension , 2002, Trends in Cognitive Sciences.

[57]  Morten H. Christiansen,et al.  Reassessing working memory: comment on Just and Carpenter (1992) and Waters and Caplan (1996). , 2002, Psychological review.

[58]  M. Mesulam.  Primary progressive aphasia—differentiation from Alzheimer's disease , 1987, Annals of neurology.

[59]  Y. Grodzinsky.  The neurology of syntax: Language use without Broca's area , 2000, Behavioral and Brain Sciences.

[60]  M. Just,et al.  The psychology of reading and language comprehension , 1986 .

[61]  Fred L. Bookstein,et al.  “Voxel-Based Morphometry” Should Not Be Used with Imperfectly Registered Images , 2001, NeuroImage.

[62]  L. Cupples,et al.  When task demands induce “asyntactic” comprehension: A study of sentence interpretation in aphasia , 1993 .

[63]  S. Bookheimer,et al.  Form and Content Dissociating Syntax and Semantics in Sentence Comprehension , 1999, Neuron.

[64]  M. Just,et al.  From the Selectedworks of Marcel Adam Just Brain Imaging of Tongue-twister Sentence Comprehension: Twisting the Tongue and the Brain Brain Imaging of Tongue-twister Sentence Comprehension: Twisting the Tongue and the Brain , 2022 .

[65]  M. Just,et al.  The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing. , 2001, Cerebral cortex.

[66]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[67]  E E Smith,et al.  Components of verbal working memory: evidence from neuroimaging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[68]  S E Petersen,et al.  A positron emission tomography study of the short-term maintenance of verbal information , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[70]  M. Hallett,et al.  Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) , 1996, Neurology.

[71]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

[72]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.